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Ossification Center of the Humeral Shaft in the Human Fetus: a CT, Digital, and Statistical Study

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Ossification Center of the Humeral Shaft in the Human Fetus: a CT, Digital, and Statistical Study Surg Radiol Anat DOI 10.1007/s00276-017-1849-4 ORIGINAL ARTICLE Ossification center of the humeral shaft in the human fetus: a CT, digital, and statistical study Marcin Wiśniewski1 · Mariusz Baumgart1 · Magdalena Grzonkowska1 · Bogdan Małkowski2 · Arnika Wilińska‑Jankowska3 · Zygmunt Siedlecki4 · Michał Szpinda1 Received: 20 September 2016 / Accepted: 16 March 2017 © The Author(s) 2017. This article is an open access publication Abstract diameter, y = −10.037 + 4.648 × ln (age) ± 0.560 for its dis- Purpose The knowledge of the development of the tal transverse diameter, y = −146.601 + 11.237 × age ± 19.9 humeral shaft ossification center may be useful both in 07 for its projection surface area, and y = 121.159 + 0.001 × determining the fetal stage and maturity and for detecting (age)4 ± 102.944 for its volume. congenital disorders, as well. This study was performed to Conclusions With no sex differences, the ossification quantitatively examine the humeral shaft ossification center center of the humeral shaft grows logarithmically with with respect to its linear, planar, and volumetric parameters. respect to its length and transverse diameters, linearly with Materials and method Using methods of CT, digital respect to its projection surface area, and fourth-degree image analysis, and statistics, the size of the humeral shaft polynomially with respect to its volume. The obtained mor- ossification center in 48 spontaneously aborted human phometric data of the humeral shaft ossification center are fetuses aged 17–30 weeks was studied. considered normative for respective prenatal weeks and Results With no sex differences, the best-fit growth may be of relevance in both the estimation of fetal ages and dynamics for the humeral shaft ossification center was mod- the ultrasonic diagnostics of congenital defects. eled by the following functions: y = −78.568 + 34.114 × ln (age) ± 2.160 for its length, y = −12.733 + 5.654 × ln­­ Keywords Humeral shaft · Ossification center · Size · (age) ± 0.515 for its proximal transverse diameter, y = Growth dynamics · Human fetus −4.750 + 2.609 × ln (age) ± 0.294 for its middle transverse * Michał Szpinda Introduction [email protected] Due to its early and intensive growth, the skeletal system in 1 Department of Normal Anatomy, The Ludwik Rydygier the fetus may effectively and safely be monitored in utero Collegium Medicum in Bydgoszcz, The Nicolaus by ultrasound at any period of gestation. However, Victo- Copernicus University in Toruń, Łukasiewicza 1 Street, Bydgoszcz 85-821, Poland ria et al. [32, 33] reported ultrasonography to be a tech- nique of 40–60% sensitivity in skeletal dysplasias. Thus, 2 Department of Positron Emission Tomography and Molecular Imaging, The Ludwik Rydygier Collegium low-dose computerized tomography may play a conducive Medicum in Bydgoszcz, The Nicolaus Copernicus University role in cases of suspected fetal skeletal dysplasia, when no in Toruń, Bydgoszcz, Poland specific diagnosis is achieved by ultrasound only [31–33]. 3 Clinic of Rheumatology and Systemic Connective Tissue Ulla et al. [31] recommended taking up further studies on Disorders, J. Biziel University Hospital No. 2, The Ludwik the clinical use of low-dose CT in fetuses and its risk–ben- Rydygier Collegium Medicum in Bydgoszcz, The Nicolaus efit analysis. Since the primary ossification centers in the Copernicus University in Toruń, Bydgoszcz, Poland 4 humeral and femoral shafts calcify as early as at week 7 of Department of Neurosurgery, Neurotraumatology prenatal life, both may ultrasonically be visualized as the and Pediatric Neurosurgery, The Ludwik Rydygier Collegium Medicum in Bydgoszcz, The Nicolaus Copernicus University first fetal structures, thus allowing both the assessment of in Toruń, Bydgoszcz, Poland fetal age and detection of potential developmental defects Vol.:(0123456789)1 3 Surg Radiol Anat [12]. Although in the assessment of fetal age the priority Materials and methods is given to the femoral length (FL), the humeral length (HL) becomes important for assessing fetal ages in the sec- The study material comprised 48 human fetuses of both ond and third trimesters of pregnancy in problematic cases sexes (26 males and 22 females) aged 17–30 weeks, orig- [15–17]. inating from spontaneous abortions or preterm deliveries. Skeletodysplasias display a large and heterogeneous All fetuses were preserved by immersion in 10% neutral group of genetic defects, in which the defective structure formalin solution. Fetal ages were previously established of bones and cartilages is a consequence of their incorrect on the base of the specimen’s crown–rump length [3]. growth, development, or differentiation. The overall inci- Each crown–rump length measurement was performed dence of skeletal dysplasias is 1 case in 5000 live births, by one researcher but three times under the same condi- which constitutes as many as 5% of children affected by tions at different times, and then averaged. The material congenital defects [12, 13]. In the diagnostics of skeleto- was acquired before the year 2000 and remains part of dysplasias, a comprehensive identification and evaluation the specimen collection of our Department of Normal of long bones is indispensable, particularly since in cases Anatomy. The experiment was approved by the Bioeth- of achondroplasia and nanism, dysplasia is limited to one ics Committee of our University (KB 275/2011). Table 1 bone only. In the upper limb, dysplasias can affect all bones lists the characteristics of the study group, including age, (micromelia), only the humerus (rhizomelia), the bones of number, and sex of the fetuses. the forearm (mesomelia), or the bones of the hand (acrome- Using the Siemens Biograph 128 mCT camera, the lia). Diagnosing both rhizomelia and mesomelia requires fetuses were scanned at a step of 0.4 mm, recorded in comparing the size of the appropriate homologous bones DICOM formats (Fig. 1), and subsequently subjected to in the upper and lower limbs: humerus with femur, radius morphometric analysis with the use of the OsiriX 3.9 with tibia, and ulna with fibula [7, 8, 11, 13]. software. It should be emphasized that OsiriX 3.9 per- In the present study, we aimed to mits precise numerical analysis of any type of linear, pla- nar, and three-dimensional reconstructions of the studied • perform morphometric analysis of the humeral shaft objects. ossification center in human fetuses with respect to its The gray scale in Hounsfield units of achieved CT linear, planar, and spatial parameters in order to deter- pictures ranged from −275 to −134 for a minimum, and mine their normative specific-age values; from +1165 to +1558 for a maximum. Thus, the window • examine possible differences between sexes for all ana- width (WW) alternated from 1.404 to 1.692, and the win- lyzed parameters; and dow level (WL) varied from +463 to +712. The details • compute growth dynamics for the analyzed parameters, of the imaging protocol were as follows: mAs—60, expressed by best-matched mathematical models. kV—80, pitch—0.35, FoV—180, and rot. time—0.5 s, Table 1 Age, number, and sex Gestational age Crown–rump length (mm) Number of Sex of the fetuses studied fetuses Weeks (Hbd-life) Mean SD Min Max ♂ ♀ 17 116.00 1.00 115.0 117.0 3 1 2 18 133.33 5.77 130.0 140.0 3 1 2 19 150.60 2.97 146.0 154.0 5 2 3 20 159.00 1.00 158.0 160.0 3 2 1 21 174.75 2.87 171.0 178.0 4 3 1 22 184.00 1.41 183.0 185.0 2 1 1 23 196.33 1.15 195.0 197.0 3 1 2 24 209.33 3.44 205.0 213.0 6 4 2 25 214.33 1.53 213.0 216.0 3 1 2 26 230.33 4.62 225.0 233.0 3 1 2 27 238.40 2.79 235.0 241.0 5 5 0 28 249.50 0.71 249.0 250.0 2 1 1 29 253.00 0.00 253.0 253.0 2 0 2 30 263.25 1.26 262.0 265.0 4 3 1 Total 48 26 22 1 3 Surg Radiol Anat Fig. 1 A male human fetus aged 21 weeks in the transverse projection (a), its skeletal recon- struction (b), its right and left upper limbs in the lateral pro- jection (c, d), its visualization referring to the left humerus (e), and humeral shaft ossification center (f) using OsiriX 3.9 while the details of CT data were as follows: slice thick- ness—0.4 mm, image increment—0.6 mm, and kernel— B45 f-medium. Despite the cartilaginous stage, contours of the proxi- mal and distal ends of the humeral shaft ossification center were already clearly visible, thus enabling a pre- cise morphometric analysis of its linear, planar, and volu- metric parameters [3]. Measurements of the humeral shaft ossification center were conducted in a specific sequence (Fig. 2). In each fetus, the assessment of linear diameters, projection surface area, and volume of the humeral shaft ossifica- tion center was carried out. In all, the following six parameters of the humeral shaft ossification center were evaluated: 1. length, based on the determined distance between the proximal and distal borderlines of the ossification center in the frontal plane (Fig. 2); 2. proximal transverse diameter, based on the determined distance between the medial and lateral borderlines of the proximal region of the ossification center in the frontal plane (Fig. 2); Fig. 2 Measurement scheme of the humeral shaft ossification center in the frontal plane. 1 length, 2 proximal transverse diameter, 3 mid- 3. middle transverse diameter, based on the determined dle transverse diameter, 4 distal transverse diameter, 5 projection sur- distance between the medial and lateral borderlines of face area 1 3 Surg Radiol Anat the central region of the ossification center in the fron- the analyzed parameters was based on linear and curvilin- tal plane (Fig.
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